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Article

Genome-Wide Association Study Identifies Two Loci for Stripe Rust Resistance in a Durum Wheat Panel from Iran

by
Ali Ashraf Mehrabi
1,*,
Brian J. Steffenson
2,*,
Alireza Pour-Aboughadareh
3,
Oadi Matny
2 and
Mahbubjon Rahmatov
4
1
Department of Plant Biotechnology, Research Institute of Forests and Rangelands, Agricultural Research, Education and Extension Organization (AREEO), Tehran 14968-13111, Iran
2
Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108, USA
3
Seed and Plant Improvement Institute, Agricultural Research, Education and Extension Organization (AREEO), Karaj 31587-77871, Iran
4
Department of Plant Breeding, Swedish University of Agricultural Sciences, Alnarp, 234 22 Lomma, Sweden
*
Authors to whom correspondence should be addressed.
Appl. Sci. 2022, 12(10), 4963; https://0-doi-org.brum.beds.ac.uk/10.3390/app12104963
Submission received: 6 March 2022 / Revised: 23 March 2022 / Accepted: 25 March 2022 / Published: 13 May 2022
(This article belongs to the Special Issue Applications of Advanced Genomic and Phenomic Technologies for Plant Improvement II)
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Abstract

:
Stripe rust (Puccinia striiformis f. sp. tritici (Pst)) is one of the most devastating fungal diseases of durum wheat (Triticum turgidum L. var. durum Desf.). Races of Pst with new virulence combinations are emerging more regularly on wheat-growing continents, which challenges wheat breeding for resistance. This study aimed to identify and characterize resistance to Pst races based on a genome-wide association study. GWAS is an approach to analyze the associations between a genome-wide set of single-nucleotide polymorphisms (SNPs) and target phenotypic traits. A total of 139 durum wheat accessions from Iran were evaluated at the seedling stage against isolates Pstv-37 and Pstv-40 of Pst and then genotyped using a 15K SNP chip. In total, 230 significant associations were identified across 14 chromosomes, of which 30 were associated with resistance to both isolates. Furthermore, 17 durum wheat landraces showed an immune response against both Pst isolates. The SNP markers and resistant accessions identified in this study may be useful in programs breeding durum wheat for stripe rust resistance.

1. Introduction

Based on estimation by UN-FAO, the global demand for agricultural products will increase by 50% by 2050 [1]. Meeting this challenge will require significant improvement in the rates of genetic gain in grain yield for cereal crops such as wheat, rice, barley, and maize, as well as the development of new cultivars that adapted to different environments and their stresses. Undoubtedly, wheat is one of the key cereals that supplies the main portion of food demand worldwide.
Durum wheat (Triticum turgidum L. var. durum Desf.), with a genomic constitution of AABB, is an economically important tetraploid cereal crop widely cultivated in the Mediterranean basin with a yearly production average of 40 million tonnes [2]. According to the International Grains Council [3], durum wheat comprises 5% of total wheat production over a cultivation area of 16 million hectares worldwide [3]. Bread and durum wheat together account for about 20% of calories and protein consumed by humans and are therefore important components of the diet [4,5]. In durum wheat’s primary cultivation area in the Mediterranean basin, crop productivity is strongly affected by various environmental stresses, such as drought, salinity, heat, etc. Moreover, recent changes in climate have exacerbated these negative effects on durum wheat production. Biotic stresses can also reduce the productivity of durum wheat in this region [6]. Among the many biotic stresses affecting the crop, stripe rust or yellow rust (causal agent: Puccinia striiformis Westend. f. sp. tritici Erikss. (Pst)) can be particularly devastating. When the plants are attacked by this disease, their leaves sustain severe damage, disrupting energy capture and contributing to premature senescence. Losses in grain yield due to stripe rust can be as high as 70% during epidemics [7,8,9].
In many countries, resistance to stripe rust is one of the most important priorities in wheat breeding programs. Resistance to stripe rust of wheat is usually classified into two categories: (i) seedling resistance (also called all-stage resistance or ASR) and (ii) adult plant resistance (APR) [10]. Seedling resistance confers a higher resistance level than APR, but is race-specific and therefore easily overcome by new virulence types arising in pathogen populations [11]. In contrast, APR is best recognized in mature plants, is partial in its effect, non-race-specific, and more durable. Over 84 Yr (yellow rust) resistance genes have described in wheat, of which only 12 have been identified in durum wheat [12,13]. Tetraploid wheats such as T. dicoccoides, and T. turgidum possess a high level of genetic diversity for agronomically important traits and may be useful as sources of stripe rust resistance genes [14]. Indeed, several important Yr genes have been described in durum wheat, including Yr15 (T. dicoccoides), Yr26 (T. turgidum), Yr35, and Yr36 (T. dicoccoides), etc. [13]. Over the last few decades, many other genes and quantitative trait loci (QTL) for stripe rust resistance have been identified and are being used in wheat breeding programs [15]. These resistances are critical for ensuring reliable production of durum wheat under the threat of future stripe rust epidemics.
Genome-wide association study (GWAS) is a genomic tool for detecting associations between target traits and genetic variants based on linkage disequilibrium (LD) in natural populations. Obtaining information on the genetic architecture of traits in a short period of time and at a lower cost are the main advantages for using GWAS in breeding programs [15]. This genetic approach has been successfully used in many studies of human, animal, and plant research. In many crops, GWAS has been widely applied for identifying QTLs for agronomic traits such as grain yield and its related components, biochemical activities, root system architecture, physiological features as well as tolerance/resistance to abiotic and biotic stresses [16,17,18,19,20,21,22,23]. GWAS has been used more extensively in wheat than almost any other crop. One of the possible reasons for this may be the availability of a reference genome sequence facilitated by the International Wheat Genome Sequencing Consortium (IWGSC), which has greatly facilitated the detection of loci associated with target traits [24]. Additionally, the availability of SNP chips with a wide range of markers (from 9K to 820K) has greatly facilitated high throughput genotyping and the construction of high-resolution maps for targeting genes underpinning both qualitative and quantitative traits in wheat [25]. In this study, we employed GWAS to identify loci for stripe rust resistance in a highly diverse and unique durum wheat panel using the Illumina iSelect 15K wheat array.

2. Materials and Methods

2.1. Genetic Materials

One hundred and twenty-three durum wheat accessions from Iran were used in this investigation. These accessions were mostly landraces selected for the panel based on their diverse agro-morphological traits from previous studies. Additionally, sixteen other accessions from the former Yugoslavia, Afghanistan, Portugal, Bulgaria, Argentina, Australia, and Iraq also were included in the study. Additional passport information is presented in Table 1.

2.2. Disease Evaluations

Seeds of each durum accession were planted and grown in cone racks of 98 cones per rack in a temperature-controlled greenhouse at 22 ± 2 °C. Three seeds were planted in each cone per accession and replicated three times. Seven to 10 days after planting, the primary leaves of seedlings were inoculated with a suspension of Pst urediniospores in a lightweight mineral oil. The panel was tested with Pst races Pstv-37 and Pstv-40 and the reaction of genotypes were categorized in four classes (R, MR, MS & S). Descriptive statistic of panel responses are illustrated in Figure 1. Immediately after inoculation, the oil carrier was allowed to fully evaporate from the plants. Then, they were placed overnight in a dew chamber at 10 °C for 24 h in the dark. After the infection period, plants were kept in growth chamber with a diurnal temperature regime of 20 ± 2 °C for 18 h in the light and 18 ± 2 °C for 6 h in the dark. The assessment of stripe rust infection types (IT) was based on the standard 0 to 9 scale described by Line et al. (1992) [26]. ITs of 0 to 6 were considered indicative of a resistant response and 7 to 9 as a susceptible response.

2.3. DNA Isolation and Genotyping Assay

The total genomic DNA was extracted from fresh, young leaves of each accession following the method of Doyle and Doyle [27]. The quality of isolated DNA was determined using electrophoresis on a 1% agarose gel. All accessions were genotyped using the wheat 15K Illumina SNP chip [28]. Markers with minor allele frequency (MAF) less than 5% and missing values of more than 10% were removed from subsequent analysis. A total of 6280 SNPs were scored and used in the final association analysis.

2.4. GWAS Analysis

Analysis of population structure in the panel was performed using STRUCTURE software ver. 2.3.4 [29] and generated the Q matrix. This analysis was done with a total of 100,000 MCMC (Markov Chain Monte Carlo) iterations and a burn-in-length of 100,000 for each K. For each K value, 10 independent runs were carried out. The relative kinship (K) matrix was estimated using TASSEL software ver 5.2.32 [30]. Linkage disequilibrium (LD) was calculated using 6280 SNPs with known map positions across the 14 durum wheat chromosomes. Squared allele frequency correlations (r2) between markers were used to estimate pairwise LD values. GWAS analysis between phenotypic data (Average of IT scores in evaluated replications) and SNP marker data was done based on a mixed linear model (MLM) incorporating genotypes, phenotypes and Q and K matrices [MLM (Q + K)]. A LOD value > 3 was used as a threshold p-value for SNP-marker-trait associations [31].

3. Results

3.1. Response of Durum Wheat Genotypes to Stripe Rust (SR)

The number and percent of accessions giving R, MR, MS, and S reactions to the two Pst races are given in Figure 1. Of the 139 accessions investigated, 33 (23.7%) and 7 (5.0%) were resistant; 57 (41.0%) and 54 (38.8%) were moderately resistant; 23 (16.5%) and 39 (28.0%) were moderately susceptible; and 28 (20.1%) and 39 (28.0%) were susceptible to races Pstv40 and Pstv-37, respectively. Figure 1 shows that 18 (12.9%), 10 (7.2%), 30 (21.6%), and 21 (15.1%) accessions were resistant, moderately resistant, moderately susceptible, and susceptible to both races, respectively. The responses of each accession against the two Pst races is presented in Table 1.

3.2. Population Structure

Population structure analysis showed that the durum wheat panel was comprised of five subpopulations (SPs) with 22, 44, 8, 18, and 30 accessions (Figure 2). Seventeen accessions did not belong to any subpopulation. Accessions resistant to one or both races were found in each subpopulation. The genetic divergence among the identified SPs was estimated through pairwise FST and varied between 0.30 (SP 3) and 0.78 (SP 1). With respect to genetic distance between SPs, SP 1 and SP 5 had the largest distance (0.29), whereas SP 2 with both SP 3 and SP 5 has the smallest distance (0.16).

3.3. LD Decay Analysis and Markers Significantly Associated with Stripe Rust Resistance

All chromosomes fell into five groups based on the genetic distance between them (Table 2). The markers with distance <5 cM showed the highest values for LD. Within this group, the highest LD was observed for chromosome 6A, while the lowest LD was found for chromosomes 1B and 6B. Chromosomes 3A, 5B, and 5A had the highest LD values when inter-marker distances were >50 cm. To identify genomic regions associated with SR resistance, we conducted a GWAS using 6280 SNP markers with a mixed linear model (MLM) on the 139 accessions. As shown in the Manhattan plots and quantile-quantile (Q-Q) plots, the MLM model was well fitted to the data and showed less deviation from the expected p-values (plots not shown).
A total of 6280 markers were utilized for GWAS of stripe rust responses, and 230 markers were found significant. One hundred and fifty-three SNPs were significantly associated with resistance to Pstv-37, among which 100 were distributed across the B sub-genome and 53 across the A sub-genome. Chromosomes 5B, 6B, and 7B contained the greatest number of significant markers within the B sub-genome with 16, 21, and 29, respectively. With respect to sub-genome A, chromosomes 1A and 4A had the greatest number of significant SNPs with 13 and 10, respectively. Seventy-seven significant associated markers were found in response to race for Pstv-40. Chromosomes 4A, 1A, and 3B had the greatest number of significant associated SNP markers with both races, respectively. A summary of the marker associations for stripe rust resistance to the two races of Pst is presented in Table S1. The percentage of phenotypic variation (R2) accounted for by significant SNPs ranged from 4 to 18%. Only three marker-trait associations showed an R2 higher than 10% (Table S1). Of the 230 marker-trait associations identified in this study, only 30 were found in response to both races of Pst (Table 3).

4. Discussion

The development of new genomic tools can facilitate advances in breeding technology, leading to greatly improved crop varieties that can, in turn, enhance global food security under the challenges of climate change [32]. Biotic stresses are one of the many consequences arising from changes in climate [33]. Stripe rust is considered one of the most important biotic stresses that can negatively affect wheat production worldwide [34]. Hence, it is important to screen wheat germplasm in response to the different virulence types of Pst present in different regions of the world [35].
In this study, we evaluated a panel of unique durum wheat landraces, predominating from Iran, to two races of Pst at the seedling stage in the glasshouse. We observed a high level of phenotypic variation among the tested accessions (Table 1), a result consistent with previous reports on the response of durum wheat germplasm to stripe rust [12,23,36,37,38]. Landraces and crop wild relatives are considered rich sources of new genes and alleles for traits in breeding programs given their high level of genetic diversity [39]. In this investigation, about one half of the evaluated landraces showed a range of responses from resistant to moderately resistant to both Pst races (Figure 1). Although most of the durum landraces included in this work were sampled from Iran, several others collected from Italy (5 samples), Portugal (1 sample), Argentina (1 sample), and Iraq (1 sample) also were resistant or moderately resistant to races Pstv-37 and Pstv-40 (Table 1).
Genetic diversity is a key requirement in any breeding program. Thus, estimation of the extent of genetic diversity and evaluation of natural population structure are important parameters for initiating genetic studies and utilizing plant genetic resources in breeding programs [40]. Population structure is an important factor for association analysis [41]. The results from STRUCTURE analysis using SNP data indicated that the durum panel was comprised of five sub-groups (Figure 2) and that 17 accessions (12%) showed a level of admixture. The grouping of the durum landraces into subpopulations was not in accordance with their geographic origins. Previously, Mehrabi et al. [22] reported a high level of molecular and morphological diversity in durum germplasm from Iran. In a study conducted by Lin et al. [42], a high level of genetic diversity was found using SNP data in a durum wheat population. In an investigation of genetic diversity within a global set of durum landraces, Kabbaj et al. [43] reported a high level of genetic variability using SNP markers.
After revealing a high level of genetic variability in the durum panel, we used a MLM model to incorporate population structure results with phenotypic data in the GWAS analysis to reduce false positive errors [44]. Based on the Q-Q plot, false positive associated markers could be successfully minimized in the association analysis of stripe rust reactions. Linkage disequilibrium (LD) is an important factor in the determination of the power of GWAS. In the present study, LD values were estimated for all chromosomes of the two sub-genomes A and B (Table 2). Like other studies, we found more rapid decay of LD in the A sub-genome compared to the B and D sub-genomes [23,45,46,47].
Based on a total of 6642 SNP markers, 230 significant associations were found for reaction to Pst races Pstv-37 and Pstv-40. Most of the associated markers for reaction to race Pstv-37 were located on the B genome, while most for reaction to race Pstv-40 were positioned on the A genome (Table S1). A recent meta-QTL analysis revealed that most stripe rust resistance loci are located on the B genome [48], which agrees with the results from the current study. Additionally, Pradhan et al. [23] identified more QTLs/defense genes against stripe rust on the B genome than on the other sub-genomes of bread wheat. In another study, Kumar et al. [49] also reported a high number of significant marker-trait associations on different chromosomes of the B sub-genome.
The R2 values for the detected associations were low to moderate (range of 3.7% and 17.8%). The three significant associations found with markers IAAV5873, tplb0033f11_1381, and Tdurum_contig10100_523 explained a high level of variation (R2 values 18%, 14%, and 11%, respectively) for reaction to race Pstv-37 (Table S1). This may be attributed to markers capturing complex allelic interactions and/or specific alleles [50]. Among the 230 significantly associated SNP markers identified in this study, 30 conferred resistances to both Pst races (Table 3). Loci conferring resistance to multiple Pst races are more desirable in breeding programs. Moreover, the multiple significant associations were mainly located on chromosomes 1A, 4A, 5A, 6A, 1B, 2B, 6B, and 7B. Many other studies have also reported these chromosomes to harbor a large number of significant MTAs and QTLs for stripe rust resistance. For instance, Zegeye et al. [51] identified several stripe rust resistance QTLs on 2B and 5A. Muleta et al. [52] identified stripe rust resistance QTLs on 1B and 2B. Furthermore, Ye et al. [53] identified several important QTLs on the long arms of 1B, 5A, 1A, 5A, 6A, and 6B. Li et al. [15] had also reported one QTL on 1B in durum wheat which confers adult plant resistance. Recently, Pradhan et al. [20] mapped several QTLs at different genomic locations, i.e., 1B, 1A, and 6B.

5. Conclusions

Durum wheat is considered a major crop in the Mediterranean region. Identification of novel alleles for stripe rust resistance is a key requirement for enhancing the resistance of new cultivars. In this study, we found a high level of variation for stripe rust resistance in a durum wheat panel originating mostly from Iran. Population stratification refers to differences in allele frequencies among extracted sub-populations due to systematic differences in ancestry rather than the association of markers with traits. Consideration of genetic structure coefficients along with a kinship matrix of genotypes is an important technical procedure that was carried out in this work to significantly reduce the rate of false positives. Within the investigated germplasm, 40 accessions (23 Iranian and 5 foreign) were immune against race Pstv-40, while 37 samples (16 Iranian and 5 foreign) were immune against race Pstv-37. Hence, this germplasm may be useful in programs aimed at pyramiding genes to achieve more durable stripe rust resistance. Our data also revealed 30 significant marker-trait associations for both races of Pst used in this study. These markers may be useful for breeders employing marker-assisted selection for stripe rust resistance. Ongoing research in this area will facilitate further advances in genomic selection using informative markers for stripe rust resistance and their application in the rapid screening of resilient genotypes for breeding programs.

Supplementary Materials

The following supporting information can be downloaded at: https://0-www-mdpi-com.brum.beds.ac.uk/article/10.3390/app12104963/s1. Table S1: List of significant SNP markers associated with two isolates of stripe rust.

Author Contributions

Conceptualization, A.A.M., B.J.S.; methodology, A.A.M.; investigation, A.A.M., O.M. and M.R.; writing—original draft preparation, A.P.-A. and A.A.M.; writing—review and editing, A.P.-A., A.A.M. and B.J.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported in part by the Minnesota Agricultural Experiment Station Project No. MIN-22-085. Open access funding is provided by the University of Minnesota.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Applsci 12 04963 g001 550
Figure 1. Summary of the frequency distribution for stripe rust reaction in 139 durum wheat accessions to two races of Pst at the seedling stage.
Figure 1. Summary of the frequency distribution for stripe rust reaction in 139 durum wheat accessions to two races of Pst at the seedling stage.
Applsci 12 04963 g001
Applsci 12 04963 g002 550
Figure 2. Population structure analysis based on 139 durum wheat accessions and 6280 SNP markers.
Figure 2. Population structure analysis based on 139 durum wheat accessions and 6280 SNP markers.
Applsci 12 04963 g002
Table
Table 1. Passport and disease reaction data of durum wheat landraces used in a genome-wide association study of stripe rust resistance.
Table 1. Passport and disease reaction data of durum wheat landraces used in a genome-wide association study of stripe rust resistance.
No.Gene Bank CodeRegionPstv-37Pstv-40No.Gene Bank CodeRegionPstv-37Pstv-40
1IUGB-00650Iran, MoghanMSMR71IUGB-00720Iran, UnknownMSMS
2IUGB-00651Iran, GorganRR72IUGB-00721Iran, UnknownSS
3IUGB-00652Iran, MianehMSMR73IUGB-00722Iran, UnknownRR
4IUGB-00653Iran, ShirvanSS74IUGB-00723Iran, UnknownMSMR
5IUGB-00654Iran, UnknownMSS75IUGB-00724Iran, UnknownSS
6IUGB-00655Iran, UnknownSMR76IUGB-00726Iran, UnknownSS
7IUGB-00656Iran, UnknownSMS77IUGB-00727Iran, UnknownRR
8IUGB-00657Iran, MashhadSS78IUGB-00728Iran, BamRMS
9IUGB-00658Iran, MashhadSS79IUGB-00729IraqRR
10IUGB-00659Iran, MashhadMSR80IUGB-00730Iran, ShoushtarMSMS
11IUGB-00660Iran, MashhadMSMS81IUGB-00731Iran, KermanshahRS
12IUGB-00661Iran, MashhadMSMR82IUGB-00732Iran, KermanshahMSS
13IUGB-00662Iran, MashhadSMS83IUGB-00733Iran, GolpayganSS
14IUGB-00663Iran, MashhadSMS84IUGB-00734Iran, UnknownSMS
15IUGB-00664Iran, MashhadSMS85IUGB-00735Iran, UnknownSMS
16IUGB-00665Iran, MashhadMRMR86IUGB-00736Iran, UnknownMSMS
17IUGB-00666Iran, MashhadSMS87IUGB-00737 Iran, UnknownMRR
18IUGB-00667Iran, GaluranSMS88IUGB-00738 Iran, UnknownMSR
19IUGB-00668Iran, GaluranSS89IUGB-00740 Iran, MashhadSS
20IUGB-00669Iran, KabkaliSMS90IUGB-00741 Iran, MashhadMRMS
21IUGB-00670Iran, ShetabanSS91IUGB-00742 Iran, MashhadMRR
22IUGB-00671Iran, Zigh AbadSMS92IUGB-00743 Iran, MashhadSMS
23IUGB-00672Iran, MahidashtMRR93IUGB-00744 Iran, MashhadSMS
24IUGB-00673Iran, UnknownMRMR94IUGB-00745 Iran, MashhadMSMS
25IUGB-00674Iran, SonghorRR95IUGB-00746 Iran, MashhadSS
26IUGB-00675Iran, KangavarRR96IUGB-00747 Iran, MashhadMSMS
27IUGB-00676Iran, AleshtarMSMR97IUGB-00750 Iran, MashhadRR
28IUGB-00677Iran, AznaSMS98IUGB-00751 Iran, MashhadRR
29IUGB-00678Iran, DelfanRR99IUGB-00752 Iran, MashhadRR
30IUGB-00679Iran, MehranMRMR100IUGB-00753 Iran, MashhadMRMR
31IUGB-00680Iran, ShebabMSS101IUGB-00754 Iran, MashhadRR
32IUGB-00681YugoslaviaMSMR102IUGB-00755 Iran, UnknownMSMS
33IUGB-00682AfghanistanSS103IUGB-00757 Iran, UnknownMSMS
34IUGB-00683Iran, DehgolanSMS104IUGB-00758 Iran, UnknownMSMS
35IUGB-00684Iran, MarivanSS105IUGB-00759 Iran, LorestanMSMS
36IUGB-00685PortugalRR106IUGB-00760 Iran, LorestanRR
37IUGB-00686AfghanistanSMS107IUGB-00761 Iran, UnknownSMS
38IUGB-00687BulgariaSS108IUGB-00762 Iran, PavehMSMS
39IUGB-00688ArgentinaRR109IUGB-00763 Iran, KermanshahMRMR
40IUGB-00689AustraliaMSMS110IUGB-00764 Iran, UnknownMRMS
41IUGB-00690BulgariaSMS111IUGB-00765 Iran, KermanshahMSR
42IUGB-00691Iran, LorestanMSMS112IUGB-00766 Iran, KermanshahMSMS
43IUGB-00693Iran, DezfulMRMR113IUGB-00767 Iran, KermanshahMSMS
44IUGB-00694Iran, LorestanMSMS114IUGB-00768Iran, KermanshahSMS
45IUGB-00695Iran, LorestanMSR115IUGB-00769Iran, KermanshahMSMS
46IUGB-00696Iran, LorestanSS116IUGB-00770Iran, GachsaranMRMS
47IUGB-00697Iran, LorestanSS117IUGB-00771Iran, KermanshahMSMS
48IUGB-00698Iran, LorestanRR118IUGB-00772Iran, HamadanMSS
49IUGB-00699Iran, LorestanRR119IUGB-00773Iran, EizehSR
50IUGB-00700Iran, LorestanSMS120IUGB-00774Iran, EizehSS
51IUGB-00701Iran, LorestanSMS121IUGB-00775Iran, DezfulSS
52IUGB-00702Iran, LorestanMSMS122IUGB-00776Iran, DezfulMSMR
53IUGB-00703Iran, LorestanMSMS123IUGB-00777Iran, ArdebilMSMR
54IUGB-00704Iran, KermanshahSS124IUGB-00778Iran, ArdebilSMS
55IUGB-00705Iran, KermanshahRR125IUGB-00779Iran, ArdebilMSMS
C56IUGB-00706Iran, LorestanMRMR126IUGB-00780Iran, AharMSMS
57IUGB-00707Iran, LorestanMRMR127IUGB-00781Iran, AharMSS
58IUGB-00708Iran, LorestanMSMS128IUGB-00782Iran, LorestanSMS
59IUGB-00709Iran, LorestanMSMS129IUGB-00783Iran, LorestanMSMR
60IUGB-00710Iran, LorestanMSS130IUGB-00784Iran, East AzarbayjanMSMS
61IUGB-00711Iran, UnknownMSS131IUGB-00785Iran, LorestanMSMS
62IUGB-00712Iran, LorestanMSMS132IUGB-00786ItalyMRMR
63IUGB-00713Iran, UnknownMSMS133IUGB-00787ItalyRMR
64IUGB-00714Iran, UnknownSS134IUGB-00788ItalyMRMR
65IUGB-00715Iran, UnknownMSMS135IUGB-00790ItalySMS
66IUGB-00716Iran, UnknownMSMR136IUGB-00791ItalyMRR
67IUGB-00717Iran, LorestanMSMS137IUGB-00792ItalyRR
68IUGB-00718Iran, UnknownMSS138IUGB-00793ItalyMSS
69IUGB-00718Iran, UnknownMSS139IUGB-00945Iran, Dareh ShahrMSMR
70IUGB-00719Iran, UnknownSS
IUGB, Ilam University Gene Bank; General stripe rust phenotyping classes were as follows: R = Resistant; MR = Moderately Resistant; MS = Moderately Susceptible; and S = Susceptible.
Table
Table 2. Average linkage disequilibrium (r2) at different marker distances for 139 durum wheat accessions.
Table 2. Average linkage disequilibrium (r2) at different marker distances for 139 durum wheat accessions.
ChromosomeNumbers of SNPsLength (cM)* Average Linkage Disequilibrium (r2) between Pair of Markers
D < 5 cMD = 5–10 cMD = 10–20 cMD = 20–50 cMD > 50 cM
1A1811060.2140.0940.0690.0480.035
1B249101.50.1270.0440.0430.0390.034
2A206119.70.1470.0410.0920.0370.032
2B391144.20.1490.0830.0650.0430.041
3A184163.40.2640.0990.0510.0520.047
3B3401370.1390.0520.0550.0380.035
4A168161.80.2380.0290.330.0230.039
4B1501070.1470.0440.0360.0440.048
5A193106.70.2170.0770.0490.0370.061
5B270179.60.250.0620.0380.0330.031
6A240120.20.3170.0470.1530.040.034
6B231110.40.1270.0460.0410.0380.039
7A251165.90.1490.0430.0430.0310.04
7B2671420.1450.0490.0420.0410.032
* The data presented in this table are based on LD analysis for a subset of genotyping data (3232 SNPs) with a known position on chromosomes.
Table
Table 3. List of SNP markers significantly associated with stripe rust resistance to both races Pstv-37 and Pstv-40 of Puccinia striiformis f. sp. tritici.
Table 3. List of SNP markers significantly associated with stripe rust resistance to both races Pstv-37 and Pstv-40 of Puccinia striiformis f. sp. tritici.
TraitMarkerPositionChr.MarkerPositionChr.MarkerPositionChr.
Pstv-37BobWhite_c53978_991156AIACX8074971Bwsnp_Ex_c2617_4864441614A
Pstv-401156A971B614A
Pstv-37BobWhite_c7786_376642BIACX82941167Bwsnp_Ex_c2617_4864955614A
Pstv-40642B1167B614A
Pstv-37BobWhite_c8428_346631AIACX9290971Bwsnp_Ex_c54395_57291841614A
Pstv-40631A971B614A
Pstv-37CAP7_c4064_1621085AKukri_c93635_290614Awsnp_Ex_c6044_10590220614A
Pstv-401085A614A614A
Pstv-37Ex_c5759_628631ARAC875_c5556_328451Bwsnp_Ex_c7002_120633251156A
Pstv-40631A451B1156A
Pstv-37Excalibur_c24041_794631ATdurum_contig12525_7691167Bwsnp_Ex_c7002_120633801156A
Pstv-40631A1167B1156A
Pstv-37Excalibur_c32735_603644ATdurum_contig44173_572556Bwsnp_Ex_c7550_12907422614A
Pstv-40644A556B614A
Pstv-37Excalibur_c7002_3141156ATdurum_contig47269_904556Bwsnp_Ex_c831_162506195B
Pstv-401156A556B95B
Pstv-37Excalibur_rep_c110429_5361407BTdurum_contig7981_70556Bwsnp_Ku_c16522_25425455556B
Pstv-401407B556B556B
Pstv-37GENE-0416_480971Bwsnp_Ex_c12818_20334501614Awsnp_Ku_c30381_40208899614A
Pstv-40971B614A614A
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Mehrabi, A.A.; Steffenson, B.J.; Pour-Aboughadareh, A.; Matny, O.; Rahmatov, M. Genome-Wide Association Study Identifies Two Loci for Stripe Rust Resistance in a Durum Wheat Panel from Iran. Appl. Sci. 2022, 12, 4963. https://0-doi-org.brum.beds.ac.uk/10.3390/app12104963

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Mehrabi AA, Steffenson BJ, Pour-Aboughadareh A, Matny O, Rahmatov M. Genome-Wide Association Study Identifies Two Loci for Stripe Rust Resistance in a Durum Wheat Panel from Iran. Applied Sciences. 2022; 12(10):4963. https://0-doi-org.brum.beds.ac.uk/10.3390/app12104963

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Mehrabi, Ali Ashraf, Brian J. Steffenson, Alireza Pour-Aboughadareh, Oadi Matny, and Mahbubjon Rahmatov. 2022. "Genome-Wide Association Study Identifies Two Loci for Stripe Rust Resistance in a Durum Wheat Panel from Iran" Applied Sciences 12, no. 10: 4963. https://0-doi-org.brum.beds.ac.uk/10.3390/app12104963

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